Cranial symmetry in baleen whales (Cetacea, Mysticeti) and the occurrence of cranial asymmetry throughout cetacean evolution

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• 作者：Julia M. Fahlke ; Oliver Hampe
• 关键词：Directional asymmetry ; Hearing ; 3D geometric morphometrics ; Photogrammetry
• 刊名：Naturwissenschaften
• 出版年：2015
• 出版时间：October 2015
• 年：2015
• 卷：102
• 期：9-10
• 全文大小：2,282 KB
• 参考文献：Adam PJ (2007) Morphological evolution in Cetacea: skull asymmetry and allometry of body size and prey. Dissertation, University of California
  Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Hystrix 24(1):7–14
  Allen DE, Leamy LJ (2001) 2,3,7,8-Tetrachlorodibenzo-p-dioxin affects size and shape, but not asymmetry, of mandibles in mice. Ecotoxicol 10:167–176CrossRef
  Arvy L (1977) Asymmetry in Cetaceans. Investig Cetacea 8:161–212
  Berta A, Sumich JL, Kovacs KM (2006) Marine mammals: evolutionary biology, 2nd edn. Elsevier Academic Press, London
  Bisconti M (2006) Titanocetus, a new baleen whale from the middle Miocene of northern Italy (Mammalia, Cetacea, Mysticeti). J Vertebr Paleontol 26(2):344–354CrossRef
  Clementz MT, Fordyce RE, Peek SL, Fox DL (2014) Ancient marine isoscapes and isotopic evidence of bulk-feeding by Oligocene cetaceans. Palaeogeogr Palaeoclimatol Palaeoecol 400:28–40CrossRef
  Cooper LN, Tobin LH, Vinyard CJ, Bajpai S, Thewissen JGM (2014) New applications for constrained ordination: reconstructing feeding behaviors in fossil Remingtonocetidae (Cetacea: Mammalia). In: Hembree DI, Platt BF, Smith JJ (eds) Experimental approaches to understanding fossil organisms: lessons from the living. Springer, New York, pp 89–107CrossRef
  Cranford TW, Amundin M, Norris KS (1996) Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J Morphol 228:223–285CrossRef PubMed
  Cranford TW, Krysl P, Hildebrand JA (2008) Acoustic pathways revealed: simulated sound transmission and reception in Cuvier’s beaked whale (Ziphius cavirostris). Bioinspir Biomim 3:1–10CrossRef
  Cranford TW, Elsberry WR, Van Bonn WG et al (2011) Observation and analysis of sonar signal generation in the bottlenose dolphin (Tursiops truncatus): evidence for two sonar sources. J Exp Mar Biol Ecol 407:81–96CrossRef
  Debat V, Alibert P, David P, Paradis E, Auffray J-C (2000) Independence between developmental stability and canalization in the skull of the house mouse. Proc R Soc B 267:423–430PubMedCentral CrossRef PubMed
  Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, Chichester
  Ekdale EG (2013) Inner ear structure of early mysticetes (Cetacea) from the late Oligocene of South Carolina: implications for the evolution of hearing in baleen whales. SVP annual meeting, J Vertebr Paleontol Program and Abstracts 2013:124
  Ekdale EG, Racicot RA (2015) Anatomical evidence for low frequency sensitivity in an archaeocete whale: comparison of the inner ear of Zygorhiza kochii with that of crown Mysticeti. J Anat 226:22–39CrossRef PubMed
  Fahlke JM, Gingerich PD, Welsh RC, Wood AR (2011) Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water. Proc Natl Acad Sci 108(35):14545–14548PubMedCentral CrossRef PubMed
  Falkingham PL (2012) Acquisition of high resolution three-dimensional models using free, open-source, photogrammetric software. Palaeontol Electron 15(1) 1T:15p. palaeo-electronica.org/content/93-issue-1-2012-technical-articles/92-3d-photogrammetry
  Feldhamer GA, Drickamer LC, Vessey SH, Merritt JF, Krajewski C (2007) Mammalogy: adaptation, diversity, ecology, 3rd edn. Johns Hopkins University Press, Baltimore
  Fitzgerald EMG (2006) A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc R Soc B 273:2955–2963PubMedCentral CrossRef PubMed
  Fitzgerald EMG (2012) Archaeocete-like jaws in a baleen whale. Biol Lett 8:94–96PubMedCentral CrossRef PubMed
  Fordyce RE, Barnes LG (1994) The evolutionary history of whales and dolphins. Annu RevEarth Planet Sci 22:419–455CrossRef
  Fordyce RE, Marx FG (2012) The pygmy right whale Caperea marginata: the last of the cetotheres. Proc R Soc B 280:20122645CrossRef PubMed
  Fordyce RE, de Muizon C (2001) Evolutionary history of cetaceans: a review. In: Mazin J-M, de Buffrénil V (eds) Secondary adaptation of tetrapods to life in water. Verlag Friedrich Pfeil, Munich, pp 169–233
  Frandsen MS, Galatius A (2013) Sexual dimorphism of Dall’s porpoise and harbor porpoise skulls. Mamm Biol 78:153–156
  Geisler JH, Uhen MD (2005) Phylogenetic relationships of extinct cetartiodactyls: results of simultaneous analyses of molecular, morphological, and stratigraphic data. J Mamm Evol 12:145–160CrossRef
  Geisler JH, Colbert MW, Carew JL (2014) A new fossil species supports an early origin for toothed whale echolocation. Nature 508:383–386CrossRef PubMed
  Gingerich PD (2005) Cetacea. In: Rose KD, Archibald JD (eds) Placental mammals: origin, timing, and relationships of the major extant clades. Johns Hopkins University Press, Baltimore, pp 234–252
  Gingerich PD, Ul-Haq M, Zalmout IS, Khan IH, Malkani MS (2001) Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293:2239–2242CrossRef PubMed
  Gómez-Robles A, Hopkins WD, Sherwood CC (2013) Increased morphological asymmetry, evolvability and plasticity in human brain evolution. Proc R Soc B 280:20130575. rspb.royalsocietypublishing.org/content/280/1761/20130575
  Gonzalez PN, Lotto FP, Hallgrímsson B (2014) Canalization and developmental stability of the fetal skull in a mouse model of maternal nutritional stress. Am J Phys Anthropol 154:544–553PubMedCentral CrossRef PubMed
  Hallgrímsson B, Willmore K, Dorval C, Cooper DML (2004) Craniofacial variability and modularity in macaques and mice. J Exp Zool B Mol Dev Evol 302:207–225CrossRef PubMed
  Hampe O, Baszio S (2010) Relative warps meet cladistics: a contribution to the phylogenetic relationships of baleen whales based on landmark analyses of mysticete crania. Bull Geosci 85(2):199–218CrossRef
  Heyning JE (1989) Comparative facial anatomy of beaked whales (Ziphiidae) and a systematic revision among the families of extant Odontoceti. Nat Hist Mus Los Angel Cty Contrib Sci 405:1–64
  Jojić V, Blagojević J, Vujošević M (2011) B chromosomes and cranial variability in yellow-necked field mice (Apodemus flavicollis). J Mammal 92:396–406CrossRef
  Ketten DR (1992) The marine mammal ear: specializations for aquatic audition and echolocation. In: Webster D, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 717–750CrossRef
  Ketten DR (1997) Structure and function in whale ears. Bioacoustics 8:103–136CrossRef
  Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357CrossRef PubMed
  Klingenberg CP (2015) Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods, and applications. Symmetry 7:843–934. doi:10.​3390/​sym7020843 CrossRef
  Klingenberg CP, Leamy LJ, Routman EJ, Cheverud JM (2001) Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics. Genetics 157:785–802PubMedCentral PubMed
  Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920CrossRef PubMed
  Klingenberg CP, Wetherill L, Rogers J, Moore E, Ward R, Autti-Rämö I, Fagerlund A, Jacobson SW, Robinson LK, Hoyme HE, Mattson SN, Li TK, Riley EP, Foroud T, the CIFAD Consortium (2010) Prenatal exposure alters the patterns of facial asymmetry. Alcohol 44:649–657PubMedCentral CrossRef PubMed
  Leamy LJ, Meagher S, Taylor S, Carroll L, Potts WK (2001) Size and fluctuating asymmetry of morphometric characters in mice: their associations with inbreeding and the t-haplotype. Evolution 55:2333–2341CrossRef PubMed
  Martin JA (2014) From finbacks to humpbacks: investigation of the evolutionary history of the Balaenopteridae. Thesis, San Diego State University. http://​sdsu-dspace.​calstate.​edu/​handle/​10211.​3/​115478
  McKenna MF, Cranford TW, Berta A, Pyenson N (2012) Morphology of the odontocete melon and its implications for acoustic function. Mar Mamm Sci 28:690–713CrossRef
  Mardia KV, Bookstein FL, Moreton IJ (2000) Statistical assessment of bilateral asymmetry of shapes. Biometrika 87:285–300CrossRef
  Marx FG (2011) The more the merrier? A large cladistic analysis of mysticetes, and comments on the transition from teeth to baleen. J Mammal Evol 18:77–100
  Marx FG, Buono MR, Fordyce RE, Boessenecker RW (2013) Juvenile morphology: a clue to the origins of the most mysterious of mysticetes? Naturwissenschaften 100:257–261. doi:10.​1007/​s00114-013-1012-y CrossRef PubMed
  Marx FG, Fordyce RE (2015) Baleen boom and bust: a synthesis of mysticete phylogeny, diversity and disparity. R Soc open sci 2:140434. http://​dx.​doi.​org/​10.​1098/​rsos.​140434
  Mead JG (1975) Anatomy of the external nasal passages and facial complex in the Delphinidae (Mammalia: Cetacea). Smithson Contrib Zool 207:1–72CrossRef
  Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36:235–247CrossRef
  Murakami M, Shimada C, Hikida Y, Hirano H (2014) Asymmetrical basal delphinoid skull from the upper lower Miocene Yamato Formation of Hokkaido, northern Japan: implications on evolution of cranial asymmetry and symmetry in Odontoceti. Paleontol Res 18:134–149CrossRef
  Ness AR (1967) A measure of asymmetry of the skulls of odontocete whales. J Zool 153:209–211CrossRef
  Norberg RA (1978) Skull asymmetry, ear structure and function, and auditory localization in Tengmalm’s Owl, Aegolius funereus (Linne). Philos Trans R Soc Lond B Biol Sci 282:325–410CrossRef
  Nummela S, Thewissen JGM (2008) The physics of sound in air and water. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 175–181
  Nummela S, Thewissen JGM, Bajpai S, Hussain ST, Kumar K (2004) Eocene evolution of whale hearing. Nature 430:776–778CrossRef PubMed
  Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Ann Rev Ecol Syst 17:391–421CrossRef
  Park T, Evans A, Fitzgerald EMG (2014) Toothed mysticete cochlear morphology provides evidence for a gradual specialization toward low frequency hearing and inability to echolocate. SVP annual meeting, J Vertebr Paleontol Progam and Abstracts 2014:201
  Reidenberg JS, Laitman JT (2007) Discovery of a low frequency sound source in Mysticeti (baleen whales): anatomical establishment of a vocal fold. Anat Rec 290:745–760CrossRef
  Ritsche IS, Wieder F, Hampe O (2013) Capability to use LF sound as an evolutionary advantage in opening up new habitats during a time of global ocean and climate change. Biennial Conference on the Biology of Marine Mammals, University of Otago, Dunedin, Abstract Book 2013:180
  Thewissen JGM, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales and artiodactyls. Nature 413:277–281CrossRef PubMed
  Tsai C-H, Fordyce RE (2014) Disparate heterochronic processes in baleen whale evolution. Evol Biol. doi:10.​1007/​s11692-014-9269-4
  Uhen MD (2004) Form, function, and anatomy of Dorudon atrox (Mammalia, Cetacea): an archaeocete from the middle to late Eocene of Egypt. Univ Mich Pap Paleontol 34:1–222
  Uhen MD (2010) The origin(s) of whales. Annu Rev Earth Planet Sci 38:189–219CrossRef
  White TA, Searle JB (2008) Mandible asymmetry and genetic diversity in island populations of the common shrew, Sorex araneus. J Evol Biol 21:636–641CrossRef PubMed
  Yurick DB, Gaskin DE (1988) Asymmetry in the skull of the harbour porpoise Phocoena phocoena (L.) and its relationship to sound production and echolocation. Can J Zool 66:399–402CrossRef
  Zelditch ML, Swiderski DL, Sheets HD (2012) Geometric morphometrics for biologists: a primer, 2nd edn. Elsevier Academic Press, London
  
• 作者单位：Julia M. Fahlke (1)
  Oliver Hampe (1)
  
  1. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, 10115, Berlin, Germany
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Life Sciences
  Environment
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1904

文摘

Odontoceti and Mysticeti (toothed and baleen whales) originated from Eocene archaeocetes that had evolved from terrestrial artiodactyls. Cranial asymmetry is known in odontocetes that can hear ultrasound (>20,000 Hz) and has been linked to the split function of the nasal passage in breathing and vocalization. Recent results indicate that archaeocetes also had asymmetric crania. Their asymmetry has been linked to directional hearing in water, although hearing frequencies are still under debate. Mysticetes capable of low-frequency and infrasonic hearing (<20 Hz) are assumed to have symmetric crania. This study aims to resolve whether mysticete crania are indeed symmetric and whether mysticete cranial symmetry is plesiomorphic or secondary. Cranial shape was analyzed applying geometric morphometrics to three-dimensional (3D) cranial models of fossil and modern mysticetes, Eocene archaeocetes, modern artiodactyls, and modern odontocetes. Statistical tests include analysis of variance, principal components analysis, and discriminant function analysis. Results suggest that symmetric shape difference reflects general trends in cetacean evolution. Asymmetry includes significant fluctuating and directional asymmetry, the latter being very small. Mysticete crania are as symmetric as those of terrestrial artiodactyls and archaeocetes, without significant differences within Mysticeti. Odontocete crania are more asymmetric. These results indicate that (1) all mysticetes have symmetric crania, (2) archaeocete cranial asymmetry is not conspicuous in most of the skull but may yet be conspicuous in the rostrum, (3) directional cranial asymmetry is an odontocete specialization, and (4) directional cranial asymmetry is more likely related to echolocation than hearing.